Publikationsserver der Universitätsbibliothek Marburg
Titel:Structure-function analysis of Cmu1, the secreted chorismate mutase from Ustilago maydis
Autor:Han, Xiaowei
Weitere Beteiligte: Kahmann, Regine (Prof. Dr.)
Veröffentlicht:2017
URI:https://archiv.ub.uni-marburg.de/diss/z2017/0770
DOI: https://doi.org/10.17192/z2017.0770
URN: urn:nbn:de:hebis:04-z2017-07705
DDC: Biowissenschaften, Biologie
Titel (trans.):Strukturfunktionsanalyse von Cmu1, der sekretierten U. maydis Chorismatmutase
Publikationsdatum:2018-06-26
Lizenz:https://creativecommons.org/licenses/by-nc-nd/4.0/

Dokument

Schlagwörter:
Ustilago zeae, Maisbeulenbrand, Ustilago maydis

Summary:
The basidiomycete fungus Ustilago maydis is the causative agent for smut disease of maize (Zea mays). More than 400 putative secreted proteins are encoded in the genome of U. maydis. The secreted chorismate mutase Cmu1 of U. maydis is such a translocated virulence promoting effector. The chorismate mutase activity of Cmu1 in the cytosol is proposed to lower the chorismate levels in the chloroplast where it would serve as precursor for the biosynthesis of the plant defense hormone salicylic acid (SA). The crystal structure of Cmu1 revealed several unique features in comparison to the cytoplasmic chorismate mutase Aro7p of Saccharomyces cerevisiae, including a surface exposed acidic patch, a disulfide bond, a putative fatty acid binding site and a loop region. This thesis shows, that site-directed mutagenesis affecting the acidic patch, the disulfide bond and the fatty acid binding site results in functional mutant proteins that can complement the virulence phenotype of CL13Δcmu1 strains. Wildtype Cmu1 protein purified after heterologous expression in E. coli followed a Michaelis-Menten kinetic in a chorismase mutase activity assay. Mutations in the fatty acid binding site did not alter the observed kinetic. A U. maydis triple mutant of cmu1, the isochorismatase coding gene um12021 and shy1 encoding a salicylate hydroxylase was reduced in virulence compared to any single or double mutants, suggesting an interplay of three U. maydis enzymes in suppressing SA pathway. By performing immunoprecipitation (IP) of Cmu1 from infected leave tissues followed by mass spectrometry, the maize protein Cmi1 (Cmu1 interactor 1) could be identified as an interactor. In vitro pull-down experiments confirmed the interaction between Cmu1 and Cmi1. Recombinant Cmi1 inhibited the chorismate mutase activity of Cmu1. The expression of cmi1 is strongly induced upon the infection of U. maydis, indicating that it is likely a pathogenesis related (PR) protein. Hydrogen-Deuterium exchange mass spectrometry (HDX/MS) mapped the interaction interface between Cmu1 and Cmi1, which involved the loop region of Cmu1. Truncation of the loop in Cmu1, which abolished the interaction of Cmu1 with Cmi1, showed only partial complementation of CL13Δcmu1 mutants, suggesting that the interaction between Cmu1 and Cmi1 may be relevant for the virulence of U. maydis.

Bibliographie / References

  1. Petre, B. and S. Kamoun (2014) "How Do Filamentous Pathogens Deliver Effector Proteins into Plant Cells?" Plos Biol 12 DOI: 10.1371/journal.pbio.1001801.
  2. Soyer, J. L., M. El Ghalid, N. Glaser, B. Ollivier, J. Linglin, J. Grandaubert, et al. (2014) "Epigenetic Control of Effector Gene Expression in the Plant Pathogenic Fungus Leptosphaeria maculans." Plos Genet 10 DOI: 10.1371/journal.pgen.1004227.
  3. Doehlemann, G., K. van der Linde, D. Assmann, D. Schwammbach, A. Hof, A. Mohanty, et al. (2009) "Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells." Plos Pathog 5, e1000290 DOI: 10.1371/journal.ppat.1000290.
  4. Bomberger, J. M., D. P. MacEachran, B. A. Coutermarsh, S. Y. Ye, G. A. O'Toole and B. A. Stanton (2009) "Long-Distance Delivery of Bacterial Virulence Factors by Pseudomonas aeruginosa Outer Membrane Vesicles." Plos Pathog 5 DOI: 10.1371/journal.ppat.1000382.
  5. Liu, Z. H., J. D. Faris, R. P. Oliver, K. C. Tan, P. S. Solomon, M. C. McDonald, et al. (2009) "SnTox3 Acts in Effector Triggered Susceptibility to Induce Disease on Wheat Carrying the Snn3 Gene." Plos Pathog 5 DOI: 10.1371/journal.ppat.1000581.
  6. Hemetsberger, C., C. Herrberger, B. Zechmann, M. Hillmer and G. Doehlemann (2012) "The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity." Plos Pathog 8, e1002684 DOI: 10.1371/journal.ppat.1002684 PPATHOGENS-D-11-02600 [pii].
  7. Djamei, A. and R. Kahmann (2012) "Ustilago maydis: Dissecting the Molecular Interface between Pathogen and Plant." Plos Pathog 8 DOI: 10.1371/journal.ppat.1002955.
  8. Mueller, A. N., S. Ziemann, S. Treitschke, D. Assmann and G. Doehlemann (2013) "Compatibility in the Ustilago maydis-Maize Interaction Requires Inhibition of Host Cysteine Proteases by the Fungal Effector Pit2." Plos Pathog 9 DOI: 10.1371/journal.ppat.1003177.
  9. Kong, G. H., Y. Zhao, M. F. Jing, J. Huang, J. Yang, Y. Q. Xia, et al. (2015) "The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b." Plos Pathog 11 DOI: 10.1371/journal.ppat.1005139.
  10. Tollot, M., D. Assmann, C. Becker, J. Altmuller, J. Y. Dutheil, C. E. Wegner, et al. (2016) "The WOPR Protein Ros1 Is a Master Regulator of Sporogenesis and Late Effector Gene Expression in the Maize Pathogen Ustilago maydis." Plos Pathog 12, e1005697 DOI: 10.1371/journal.ppat.1005697.
  11. Katsir, L. and O. Bahar (2017) "Bacterial outer membrane vesicles at the plant-pathogen interface." Plos Pathog 13 DOI: 10.1371/journal.ppat.1006306.
  12. Sanchez-Vallet, A., R. Saleem-Batcha, A. Kombrink, G. Hansen, D. J. Valkenburg, B. P. H. J. Thomma, et al. (2013) "Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization." Elife 2 DOI: 10.7554/eLife.00790.
  13. Tanaka, S., T. Brefort, N. Neidig, A. Djamei, J. Kahnt, W. Vermerris, et al. (2014) "A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize." Elife 3 DOI: 10.7554/eLife.01355.
  14. Cao, Y., Y. Liang, K. Tanaka, C. T. Nguyen, R. P. Jedrzejczak, A. Joachimiak, et al. (2014) "The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1." Elife 3 DOI: 10.7554/eLife.03766.
  15. Hake, S. and J. Ross-Ibarra (2015) "Genetic, evolutionary and plant breeding insights from the domestication of maize." Elife 4 DOI: 10.7554/eLife.05861.
  16. Okvist, M., R. Dey, S. Sasso, E. Grahn, P. Kast and U. Krengel (2006). "1.6 A crystal structure of the secreted chorismate mutase from Mycobacterium tuberculosis: novel fold topology revealed." J Mol Biol 357(5): 1483-1499.
  17. Rodriguez-Herva, J. J., P. Gonzalez-Melendi, R. Cuartas-Lanza, M. Antunez-Lamas, I. Rio- Alvarez, Z. Li, et al. (2012). "A bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses." Cell Microbiol 14(5): 669-681.
  18. Kamoun, S. (2006). "A catalogue of the effector secretome of plant pathogenic oomycetes." Annu Rev Phytopathol 44: 41-60.
  19. Bekal, S., T. L. Niblack and K. N. Lambert (2003). "A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence." Mol Plant Microbe Interact 16(5): 439-446.
  20. Coaker, G., A. Falick and B. Staskawicz (2005). "Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin." Science 308(5721): 548-550.
  21. Brutus, A., F. Sicilia, A. Macone, F. Cervone and G. De Lorenzo (2010). "A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides." Proc. Natl. Acad. Sci. U.S.A. 107(20): 9452-9457.
  22. Mukamolova, G. V., O. A. Turapov, D. I. Young, A. S. Kaprelyants, D. B. Kell and M. Young (2002b). "A family of autocrine growth factors in Mycobacterium tuberculosis." Mol Microbiol 46(3): 623-635.
  23. Jelenska, J., N. Yao, B. A. Vinatzer, C. M. Wright, J. L. Brodsky and J. T. Greenberg (2007). "A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses." Current Biology 17(6): 499-508.
  24. Ranf, S., N. Gisch, M. Schaffer, T. Illig, L. Westphal, Y. A. Knirel, et al. (2015). "A lectin S- domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana." Nat Immunol 16(4): 426-433.
  25. Helmstaedt, K., S. Krappmann and G. H. Braus (2001). "Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase." Microbiol Mol Biol Rev 65(3): 404-421, table of contents.
  26. Lecourieux, D., C. Mazars, N. Pauly, R. Ranjeva and A. Pugin (2002). "Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells." Plant Cell 14(10): 2627-2641.
  27. Lo Presti, L., B. Zechmann, J. Kumlehn, L. Liang, D. Lanver, S. Tanaka, et al. (2017). "An assay for entry of secreted fungal effectors into plant cells." New Phytol 213(2): 956-964.
  28. Schornack, S., M. van Damme, T. O. Bozkurt, L. M. Cano, M. Smoker, M. Thines, et al. (2010a). "Ancient class of translocated oomycete effectors targets the host nucleus." Proc. Natl. Acad. Sci. U.S.A. 107(40): 17421-17426.
  29. Schornack, S., M. van Damme, T. O. Bozkurt, L. M. Cano, M. Smoker, M. Thines, et al. (2010b). "Ancient class of translocated oomycete effectors targets the host nucleus." Proc. Natl. Acad. Sci. U.S.A. 107(40): 17421-17426.
  30. Huffaker, A., G. Pearce and C. A. Ryan (2006). "An endogenous peptide signal in Arabidopsis activates components of the innate immune response." Proc. Natl. Acad. Sci. U.S.A. 103(26): 10098-10103.
  31. Ponstein, A. S., S. A. Bresvloemans, M. B. Selabuurlage, P. J. M. Vandenelzen, L. S. Melchers and B. J. C. Cornelissen (1994). "A Novel Pathogen-Inducible and Wound-Inducible Tobacco (Nicotiana-Tabacum) Protein with Antifungal Activity." Plant Physiol 104(1): 109-118.
  32. Hejgaard, J., S. Jacobsen, S. E. Bjorn and K. M. Kragh (1992). "Antifungal Activity of Chitin- Binding Pr-4 Type Proteins from Barley-Grain and Stressed Leaf." Febs Letters 307(3): 389-392.
  33. Kämper, J. (2004). "A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis." Mol Genet Genomics 271(1): 103-110.
  34. O'Brien, J. A., A. Daudi, P. Finch, V. S. Butt, J. P. Whitelegge, P. Souda, et al. (2012). "A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense." Plant Physiol 158(4): 2013-2027.
  35. Colquhoun, T. A., B. C. J. Schimmel, J. Y. Kim, D. Reinhardt, K. Cline and D. G. Clark (2010). "A petunia chorismate mutase specialized for the production of floral volatiles." Plant J 61(1): 145-155.
  36. Ma, Z. C., T. Q. Song, L. Zhu, W. W. Ye, Y. Wang, Y. Y. Shao, et al. (2015). "A Phytophthora sojae Glycoside Hydrolase 12 Protein Is a Major Virulence Factor during Soybean Infection and Is Recognized as a PAMP." Plant Cell 27(7): 2057-2072.
  37. Sarris, P. F., Z. Duxbury, S. U. Huh, Y. Ma, C. Segonzac, J. Sklenar, et al. (2015). "A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors." Cell 161(5): 1089-1100.
  38. Doehlemann, G. and C. Hemetsberger (2013). "Apoplastic immunity and its suppression by filamentous plant pathogens." New Phytol 198(4): 1001-1016.
  39. Willmann, R., H. M. Lajunen, G. Erbs, M. A. Newman, D. Kolb, K. Tsuda, et al. (2011). "Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection." Proc. Natl. Acad. Sci. U.S.A. 108(49): 19824- 19829.
  40. Le Roux, C., G. Huet, A. Jauneau, L. Camborde, D. Tremousaygue, A. Kraut, et al. (2015). "A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity." Cell 161(5): 1074-1088.
  41. Boller, T. and G. Felix (2009). "A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors." Annu Rev Plant Biol 60: 379-406.
  42. Redkar, A., R. Hoser, L. Schilling, B. Zechmann, M. Krzymowska, V. Walbot, et al. (2015). "A Secreted Effector Protein of Ustilago maydis Guides Maize Leaf Cells to Form Tumors." Plant Cell 27(4): 1332-1351.
  43. Dutheil, J. Y., G. Mannhaupt, G. Schweizer, C. M. K. Sieber, M. Munsterkotter, U. Guldener, et al. (2016). "A Tale of Genome Compartmentalization: The Evolution of Virulence Clusters in Smut Fungi." Genome Biol Evol 8(3): 681-704.
  44. Lee, A. Y., P. A. Karplus, B. Ganem and J. Clardy (1995). "Atomic structure of the buried catalytic pocket of Escherichia coli chorismate mutase." J Am Chem Soc 117(12): 3627- 3628.
  45. Whisson, S. C., P. C. Boevink, L. Moleleki, A. O. Avrova, J. G. Morales, E. M. Gilroy, et al. (2007). "A translocation signal for delivery of oomycete effector proteins into host plant cells." Nature 450(7166): 115-118.
  46. Gillissen, B., J. Bergemann, C. Sandmann, B. Schroeer, M. Bolker and R. Kahmann (1992). "A two-component regulatory system for self/non-self recognition in Ustilago maydis." Cell 68(4): 647-657.
  47. Kuehn, M. J. and N. C. Kesty (2005). "Bacterial outer membrane vesicles and the host-pathogen interaction." Gene Dev 19(22): 2645-2655.
  48. Qi, Z., R. Verma, C. Gehring, Y. Yamaguchi, Y. Zhao, C. A. Ryan, et al. (2010). "Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels." Proc. Natl. Acad. Sci. U.S.A. 107(49): 21193-21198.
  49. Pei, Z. M., Y. Murata, G. Benning, S. Thomine, B. Klusener, G. J. Allen, et al. (2000). "Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells." Nature 406(6797): 731-734.
  50. Kobayashi, M., I. Ohura, K. Kawakita, N. Yokota, M. Fujiwara, K. Shimamoto, et al. (2007). "Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase." Plant Cell 19(3): 1065-1080.
  51. Luna, E., V. Pastor, J. Robert, V. Flors, B. Mauch-Mani and J. Ton (2011). "Callose deposition: a multifaceted plant defense response." Mol Plant Microbe Interact 24(2): 183-193.
  52. Lee, J., L. Eschen-Lippold, I. Lassowskat, C. Bottcher and D. Scheel (2015). "Cellular reprogramming through mitogen-activated protein kinases." Front Plant Sci 6: 940.
  53. Miya, A., P. Albert, T. Shinya, Y. Desaki, K. Ichimura, K. Shirasu, et al. (2007). "CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis." Proc. Natl. Acad. Sci. U.S.A. 104(49): 19613-19618.
  54. Jones, J. T., C. Furlanetto, E. Bakker, B. Banks, V. Blok, Q. Chen, et al. (2003). "Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida." Mol Plant Pathol 4(1): 43-50.
  55. Guevara-Morato, M. A., M. G. de Lacoba, I. Garcia-Luque and M. T. Serra (2010). "Characterization of a pathogenesis-related protein 4 (PR-4) induced in Capsicum chinense L3 plants with dual RNase and DNase activities." J Exp Bot 61(12): 3259-3271.
  56. Sasso, S., C. Ramakrishnan, M. Gamper, D. Hilvert and P. Kast (2005). "Characterization of the secreted chorismate mutase from the pathogen Mycobacterium tuberculosis." FEBS J 272(2): 375-389.
  57. Dopheide, T. A., B. E. Davidson and P. Crewther (1972). "Chorismate Mutase-Prephenate Dehydratase from Escherichia-Coli K-12 .2. Kinetic Properties." J Biol Chem 247(14): 4447-&.
  58. Christopherson, R. I. (1985). "Chorismate Mutase-Prephenate Dehydrogenase from Escherichia- Coli -Cooperative Effects and Inhibition by L-Tyrosine." Arch Biochem Biophys 240(2): 646-654.
  59. Rooney, H. C. E., J. W. van 't Klooster, R. A. L. van der Hoorn, M. H. A. J. Joosten, J. D. G. Jones and P. J. G. M. de Wit (2005). "Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance." Science 308(5729): 1783-1786.
  60. Laemmli, U. K. (1970). "Cleavage of structural proteins during the assembly of the head of bacteriophage T4." Nature 227(5259): 680-685.
  61. Schuster, M., G. Schweizer and R. Kahmann (2017). "Comparative analyses of secreted proteins in plant pathogenic smut fungi and related basidiomycetes." Fungal Genet Biol.
  62. Gan, P., K. Ikeda, H. Irieda, M. Narusaka, R. J. O'Connell, Y. Narusaka, et al. (2013). "Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi." New Phytol 197(4): 1236-1249.
  63. Draffehn, A. M., L. Li, N. Krezdorn, J. Ding, J. Lubeck, J. Strahwald, et al. (2013). "Comparative transcript profiling by SuperSAGE identifies novel candidate genes for controlling potato quantitative resistance to late blight not compromised by late maturity." Front Plant Sci 4: 423.
  64. Glazebrook, J. (2005). "Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens." Annu Rev Phytopathol 43: 205-227.
  65. Kahmann, R., T. Romeis, M. Bolker and J. Kamper (1995). "Control of mating and development in Ustilago maydis." Curr Opin Genet Dev 5(5): 559-564.
  66. Christensen, J. J. (1963). Corn smut caused by Ustilago maydis. Monograph 2. St. Paul (Minnesota), American Phytopathology Society: 1-40.
  67. Mazars, C., P. Thuleau, O. Lamotte and S. Bourque (2010). "Cross-Talk between ROS and Calcium in Regulation of Nuclear Activities." Molecular Plant 3(4): 706-718.
  68. Hamiaux, C., R. Maddumage, M. J. Middleditch, R. Prakash, D. A. Brummell, E. N. Baker, et al. (2014). "Crystal structure of kiwellin, a major cell-wall protein from kiwifruit." J Struct Biol 187(3): 276-281.
  69. Blondeau, K., F. Blaise, M. Graille, S. D. Kale, J. Linglin, B. Ollivier, et al. (2015). "Crystal structure of the effector AvrLm4-7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins." Plant J 83(4): 610-624.
  70. Strater, N., K. Hakansson, G. Schnappauf, G. Braus and W. N. Lipscomb (1996). "Crystal structure of the T state of allosteric yeast chorismate mutase and comparison with the R state." Proc. Natl. Acad. Sci. U.S.A. 93(8): 3330-3334.
  71. Wang, C. I. A., G. Guncar, J. K. Forwood, T. Teh, A. M. Catanzariti, G. J. Lawrence, et al. (2007). "Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity." Plant Cell 19(9): 2898-2912.
  72. Chook, Y. M., H. M. Ke and W. N. Lipscomb (1993). "Crystal-Structures of the Monofunctional Chorismate Mutase from Bacillus-Subtilis and Its Complex with a Transition-State Analog." Proc. Natl. Acad. Sci. U.S.A. 90(18): 8600-8603.
  73. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. Seidman, J. Smith, et al. (1987). Current Protocols in Molecular Biology. New York, Greene Pub. Associates and Wiley-Interscience.
  74. Reinbothe, C., B. Ortel, B. Parthier and S. Reinbothe (1994). "Cytosolic and Plastid Forms of 5-Enolpyruvylshikimate-3-Phosphate Synthase in Euglena-Gracilis Are Differentially Expressed during Light-Induced Chloroplast Development." Molecular & General Genetics 245(5): 616-622.
  75. Eberhard, J., T. T. Ehrler, P. Epple, G. Felix, H. R. Raesecke, N. Amrhein, et al. (1996b). "Cytosolic and plastidic chorismate mutase isozymes from Arabidopsis thaliana: Molecular characterization and enzymatic properties." Plant J 10(5): 815-821.
  76. Robert, X. and P. Gouet (2014). "Deciphering key features in protein structures with the new ENDscript server." Nucleic Acids Res 42(W1): W320-W324.
  77. Rabe, F., Z. Ajami-Rashidi, G. Doehlemann, R. Kahmann and A. Djamei (2013). "Degradation of the plant defence hormone salicylic acid by the biotrophic fungus Ustilago maydis." Mol Microbiol 89(1): 179-188.
  78. Banuett, F. and I. Herskowitz (1989). "Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis." Proc. Natl. Acad. Sci. U.S.A. 86(15): 5878-5882.
  79. Phan, H. T. T., K. Rybak, E. Furuki, S. Breen, P. S. Solomon, R. P. Oliver, et al. (2016). "Differential effector gene expression underpins epistasis in a plant fungal disease." Plant J 87(4): 343-354.
  80. Stanford, A., M. Bevan and D. Northcote (1989). "Differential Expression within a Family of Novel Wound-Induced Genes in Potato." Molecular & General Genetics 215(2): 200-208.
  81. Davies, C. and S. P. Robinson (2000). "Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins." Plant Physiol 122(3): 803-812.
  82. Banuett, F. and I. Herskowitz (1996). "Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis." Development 122(10): 2965-2976.
  83. Takai, S., S. A. Hines, T. Sekizaki, V. M. Nicholson, D. A. Alperin, M. Osaki, et al. (2000). "DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103." Infect Immun 68(12): 6840-6847.
  84. Kradolfer, P., J. Zeyer, G. Miozzari and R. Huetter (1977). "Dominant Regulatory Mutants in Chorismate Mutase of Saccharomyces-Cerevisiae." Fems Microbiol Lett 2(4): 211-216.
  85. Mentlak, T. A., A. Kombrink, T. Shinya, L. S. Ryder, I. Otomo, H. Saitoh, et al. (2012). "Effector-Mediated Suppression of Chitin-Triggered Immunity by Magnaporthe oryzae Is Necessary for Rice Blast Disease." Plant Cell 24(1): 322-335.
  86. Plett, J. M., Y. Daguerre, S. Wittulsky, A. Vayssieres, A. Deveau, S. J. Melton, et al. (2014a). "Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes." Proc. Natl. Acad. Sci. U.S.A. 111(22): 8299-8304.
  87. Ramachandran, S. R., C. T. Yin, J. Kud, K. Tanaka, A. K. Mahoney, F. M. Xiao, et al. (2017). "Effectors from Wheat Rust Fungi Suppress Multiple Plant Defense Responses." Phytopathology 107(1): 75-83.
  88. Franceschetti, M., A. Maqbool, M. J. Jimenez-Dalmaroni, H. G. Pennington, S. Kamoun and M. J. Banfield (2017). "Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity." Microbiol Mol Biol Rev 81(2).
  89. Pedelacq, J. D., S. Cabantous, T. Tran, T. C. Terwilliger and G. S. Waldo (2006). "Engineering and characterization of a superfolder green fluorescent protein." Nat Biotechnol 24(1): 79- 88.
  90. Plett, J. M., A. Khachane, M. Ouassou, B. Sundberg, A. Kohler and F. Martin (2014b). "Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots." New Phytol 202(1): 270-286.
  91. Berens, M. L., H. M. Berry, A. Mine, C. T. Argueso and K. Tsuda (2017). "Evolution of Hormone Signaling Networks in Plant Defense." Annu Rev Phytopathol.
  92. Bumann, D. (2002). "Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry." Mol Microbiol 43(5): 1269-1283.
  93. Sommer, S. and L. Heide (1998). "Expression of bacterial chorismate pyruvate-lyase in tobacco: Evidence for the presence of chorismate in the plant cytosol." Plant Cell Physiol 39(11): 1240-1244.
  94. Szempruch, A. J., S. E. Sykes, R. Kieft, L. Dennison, A. C. Becker, A. Gartrell, et al. (2016). "Extracellular Vesicles from Trypanosoma brucei Mediate Virulence Factor Transfer and Cause Host Anemia." Cell 164(1-2): 246-257.
  95. Rodrigues, M. L., E. S. Nakayasu, D. L. Oliveira, L. Nimrichter, J. D. Nosanchuk, I. C. Almeida, et al. (2008). "Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence." Eukaryot Cell 7(1): 58-67.
  96. Sievers, F., A. Wilm, D. Dineen, T. J. Gibson, K. Karplus, W. Z. Li, et al. (2011). "Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega." Mol Syst Biol 7.
  97. Rovenich, H., J. C. Boshoven and B. P. H. J. Thomma (2014). "Filamentous pathogen effector functions: of pathogens, hosts and microbiomes." Curr Opin Plant Biol 20: 96-103.
  98. Gomez-Gomez, L. and T. Boller (2000). "FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis." Mol Cell 5(6): 1003-1011.
  99. Sevier, C. S. and C. A. Kaiser (2002). "Formation and transfer of disulphide bonds in living cells." Nat Rev Mol Cell Biol 3(11): 836-847.
  100. van der Hoorn, R. A. and S. Kamoun (2008). "From Guard to Decoy: a new model for perception of plant pathogen effectors." Plant Cell 20(8): 2009-2017.
  101. Kovtun, Y., W. L. Chiu, G. Tena and J. Sheen (2000). "Functional analysis of oxidative stress- activated mitogen-activated protein kinase cascade in plants." Proc. Natl. Acad. Sci. U.S.A. 97(6): 2940-2945.
  102. de Wit, P. J. G. M., R. Mehrabi, H. A. van den Burg and I. Stergiopoulos (2009). "Fungal effector proteins: past, present and future." Molecular Plant Pathology 10(6): 735-747.
  103. Lo Presti, L., D. Lanver, G. Schweizer, S. Tanaka, L. Liang, M. Tollot, et al. (2015). "Fungal effectors and plant susceptibility." Annu Rev Plant Biol 66: 513-545.
  104. Banuett, F. (1995). "Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize." Annu Rev Genet 29: 179-208.
  105. Schuster, M., G. Schweizer, S. Reissmann and R. Kahmann (2016). "Genome editing in Ustilago maydis using the CRISPR-Cas system." Fungal Genet Biol 89: 3-9.
  106. Raffaele, S. and S. Kamoun (2012). "Genome evolution in filamentous plant pathogens: why bigger can be better." Nat Rev Microbiol 10(6): 417-430.
  107. Spellig, T., A. Bottin and R. Kahmann (1996). "Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis." Molecular & General Genetics 252(5): 503-509.
  108. Pieterse, C. M., D. Van der Does, C. Zamioudis, A. Leon-Reyes and S. C. Van Wees (2012). "Hormonal modulation of plant immunity." Annu Rev Cell Dev Biol 28: 489-521.
  109. Chisholm, S. T., G. Coaker, B. Day and B. J. Staskawicz (2006). "Host-microbe interactions: shaping the evolution of the plant immune response." Cell 124(4): 803-814.
  110. Lo Presti, L. and R. Kahmann (2017). "How filamentous plant pathogen effectors are translocated to host cells." Curr Opin Plant Biol 38: 19-24.
  111. Englander, S. W. (2006). "Hydrogen exchange and mass spectrometry: A historical perspective." J Am Soc Mass Spectr 17(11): 1481-1489.
  112. Konermann, L., J. X. Pan and Y. H. Liu (2011). "Hydrogen exchange mass spectrometry for studying protein structure and dynamics." Chem Soc Rev 40(3): 1224-1234.
  113. Wales, T. E. and J. R. Engen (2006). "Hydrogen exchange mass spectrometry for the analysis of protein dynamics." Mass Spectrom Rev 25(1): 158-170.
  114. Mobley, E. M., B. N. Kunkel and B. Keith (1999). "Identification, characterization and comparative analysis of a novel chorismate mutase gene in Arabidopsis thaliana." Gene 240(1): 115-123.
  115. Choi, J., K. Tanaka, Y. Cao, Y. Qi, J. Qiu, Y. Liang, et al. (2014). "Identification of a plant receptor for extracellular ATP." Science 343(6168): 290-294.
  116. Espadaler, J., E. Querol, F. X. Aviles and B. Oliva (2006). "Identification of function-associated loop motifs and application to protein function prediction." Bioinformatics 22(18): 2237- 2243.
  117. Banuett, F. and I. Herskowitz (1994). "Identification of Fuz7, a Ustilago-Maydis Mek/Mapkk Homolog Required for a-Locus-Dependent and a-Locus-Independent Steps in the Fungal Life-Cycle." Gene Dev 8(12): 1367-1378.
  118. Brachmann, A., G. Weinzierl, J. Kamper and R. Kahmann (2001). "Identification of genes in the bW/bE regulatory cascade in Ustilago maydis." Mol Microbiol 42(4): 1047-1063.
  119. Aichinger, C., K. Hansson, H. Eichhorn, F. Lessing, G. Mannhaupt, W. Mewes, et al. (2003). "Identification of plant-regulated genes in Ustilago maydis by enhancer-trapping mutagenesis." Molecular Genetics and Genomics 270(4): 303-314.
  120. Snetselaar, K. M. and C. W. Mims (1993). "Infection of Maize Stigmas by Ustilago-Maydis - Light and Electron-Microscopy." Phytopathology 83(8): 843-850.
  121. Kämper, J., R. Kahmann, M. Bolker, L. J. Ma, T. Brefort, B. J. Saville, et al. (2006). "Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis." Nature 444(7115): 97-101.
  122. Mosquera, G., M. C. Giraldo, C. H. Khang, S. Coughlan and B. Valent (2009). "Interaction Transcriptome Analysis Identifies Magnaporthe oryzae BAS1-4 as Biotrophy-Associated Secreted Proteins in Rice Blast Disease." Plant Cell 21(4): 1273-1290.
  123. Letunic, I. and P. Bork (2016). "Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees." Nucleic Acids Res 44(W1): W242-W245.
  124. Rafiqi, M., P. H. Gan, M. Ravensdale, G. J. Lawrence, J. G. Ellis, D. A. Jones, et al. (2010). "Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen." Plant Cell 22(6): 2017-2032.
  125. Kazan, K. and R. Lyons (2014). "Intervention of Phytohormone Pathways by Pathogen Effectors." Plant Cell 26(6): 2285-2309.
  126. Jones, J. D., R. E. Vance and J. L. Dangl (2016). "Intracellular innate immune surveillance devices in plants and animals." Science 354(6316).
  127. Keon, J. P. R., G. A. White and J. A. Hargreaves (1991). "Isolation, Characterization and Sequence of a Gene Conferring Resistance to the Systemic Fungicide Carboxin from the Maize Smut Pathogen, Ustilago-Maydis." Current Genetics 19(6): 475-481.
  128. Eberhard, J., M. Bischoff, H. R. Raesecke, N. Amrhein and J. Schmid (1996a). "Isolation of a cDNA from tomato coding for an unregulated, cytosolic chorismate mutase." Plant Molecular Biology 31(4): 917-922.
  129. Steinberg, G., M. Schliwa, C. Lehmler, M. Bolker, R. Kahmann and J. R. McIntosh (1998). "Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration." J Cell Sci 111 ( Pt 15): 2235-2246.
  130. Ciardiello, M. A., D. Meleleo, G. Saviano, R. Crescenzo, V. Carratore, L. Camardella, et al. (2008). "Kissper, a kiwi fruit peptide with channel-like activity: Structural and functional features." J Pept Sci 14(6): 742-754.
  131. Tuppo, L., I. Giangrieco, P. Palazzo, M. L. Bernardi, E. Scala, V. Carratore, et al. (2008). "Kiwellin, a modular protein from green and gold kiwi fruits: evidence of in vivo and in vitro processing and IgE binding." J Agric Food Chem 56(10): 3812-3817.
  132. Tamburrini, M., I. Cerasuolo, V. Carratore, A. A. Stanziola, S. Zofra, L. Romano, et al. (2005). "Kiwellin, a novel protein from kiwi fruit. Purification, biochemical characterization and identification as an allergen*." Protein J 24(7-8): 423-429.
  133. Snetselaar, K. M. and C. W. Mims (1994). "Light and Electron-Microscopy of Ustilago-Maydis Hyphae in Maize." Mycol Res 98: 347-355.
  134. Xue, Y. and W. N. Lipscomb (1995). "Location of the active site of allosteric chorismate mutase from Saccharomyces cerevisiae, and comments on the catalytic and regulatory mechanisms." Proc. Natl. Acad. Sci. U.S.A. 92(23): 10595-10598.
  135. van Wees, S. C. M. and J. Glazebrook (2003). "Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid." Plant J 33(4): 733-742.
  136. Skibbe, D. S., G. Doehlemann, J. Fernandes and V. Walbot (2010). "Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen." Science 328(5974): 89-92.
  137. Strable, J. and M. J. Scanlon (2009). "Maize (Zea mays): a model organism for basic and applied research in plant biology." Cold Spring Harb Protoc 2009(10): pdb emo132.
  138. Muller, P., G. Weinzierl, A. Brachmann, M. Feldbrugge and R. Kahmann (2003). "Mating and pathogenic development of the Smut fungus Ustilago maydis are regulated by one mitogen- activated protein kinase cascade." Eukaryot Cell 2(6): 1187-1199.
  139. Kahmann, R. and J. Schirawski (2007). Mating in the smut fungi: from a to b to the downstream cascades. Sex in Fungi. K. J. Heitman J, Taylor J, Casselton L. Washington, DC., American Society of Microbiology: 377-387.
  140. Doyle, E. A. and K. N. Lambert (2003). "Meloidogyne javanica chorismate mutase 1 alters plant cell development." Mol Plant Microbe Interact 16(2): 123-131.
  141. Kane, J. F., S. L. Stenmark, D. H. Calhoun and R. A. Jensen (1971). "Metabolic interlock. The role of the subordinate type of enzyme in the regulation of a complex pathway." J Biol Chem 246(13): 4308-4316.
  142. Djamei, A., K. Schipper, F. Rabe, A. Ghosh, V. Vincon, J. Kahnt, et al. (2011). "Metabolic priming by a secreted fungal effector." Nature 478(7369): 395-398.
  143. Tyler, B. M., S. D. Kale, Q. Wang, K. Tao, H. R. Clark, K. Drews, et al. (2013). "Microbe- independent entry of oomycete RxLR effectors and fungal RxLR-like effectors into plant and animal cells is specific and reproducible." Mol Plant Microbe Interact 26(6): 611-616.
  144. Tanaka, S., X. Han and R. Kahmann (2015). "Microbial effectors target multiple steps in the salicylic acid production and signaling pathway." Front Plant Sci 6: 349.
  145. Sambrook, J., E. F. Fritsch and T. Maniatis (1989). Molecular cloning: a laboratory manual. New York, Cold spring harbor laboratory press.
  146. Kämper, J., M. Reichmann, T. Romeis, M. Bolker and R. Kahmann (1995). "Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis." Cell 81(1): 73-83.
  147. An, Q. L., K. Ehlers, K. H. Kogel, A. J. E. van Bel and R. Huckelhoven (2006). "Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus." New Phytol 172(3): 563-576.
  148. Tzin, V. and G. Galili (2010). "New Insights into the Shikimate and Aromatic Amino Acids Biosynthesis Pathways in Plants." Molecular Plant 3(6): 956-972.
  149. Duplessis, S., C. A. Cuomo, Y. C. Lin, A. Aerts, E. Tisserant, C. Veneault-Fourrey, et al. (2011). "Obligate biotrophy features unraveled by the genomic analysis of rust fungi." P Natl Acad Sci USA 108(22): 9166-9171.
  150. Chen, D. C., B. C. Yang and T. T. Kuo (1992). "One-Step Transformation of Yeast in Stationary Phase." Current Genetics 21(1): 83-84.
  151. Hwang, I. S., D. S. Choi, N. H. Kim, D. S. Kim and B. K. Hwang (2014). "Pathogenesis-related protein 4b interacts with leucine-rich repeat protein 1 to suppress PR4b-triggered cell death and defense response in pepper." Plant J 77(4): 521-533.
  152. Friedrich, L., M. Moyer, E. Ward and J. Ryals (1991). "Pathogenesis-related protein 4 is structurally homologous to the carboxy-terminal domains of hevein, Win-1 and Win-2." Mol Gen Genet 230(1-2): 113-119.
  153. Kim, N. H. and B. K. Hwang (2015). "Pepper pathogenesis-related protein 4c is a plasma membrane-localized cysteine protease inhibitor that is required for plant cell death and defense signaling." Plant J 81(1): 81-94.
  154. Yamaguchi, Y., A. Huffaker, A. C. Bryan, F. E. Tax and C. A. Ryan (2010). "PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis." Plant Cell 22(2): 508-522.
  155. Zipfel, C., G. Kunze, D. Chinchilla, A. Caniard, J. D. Jones, T. Boller, et al. (2006). "Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation." Cell 125(4): 749-760.
  156. Mendoza-Mendoza, A., P. Berndt, A. Djamei, C. Weise, U. Linne, M. Marahiel, et al. (2009). "Physical-chemical plant-derived signals induce differentiation in Ustilago maydis." Mol Microbiol 71(4): 895-911.
  157. Stergiopoulos, I., J. Collemare, R. Mehrabi and P. J. G. M. De Wit (2013). "Phytotoxic secondary metabolites and peptides produced by plant pathogenic Dothideomycete fungi." Fems Microbiol Rev 37(1): 67-93.
  158. Dangl, J. L., D. M. Horvath and B. J. Staskawicz (2013). "Pivoting the Plant Immune System from Dissection to Deployment." Science 341(6147): 746-751.
  159. Kaffarnik, F., P. Muller, M. Leibundgut, R. Kahmann and M. Feldbrugge (2003). "PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis." Embo J 22(21): 5817-5826.
  160. Asai, S. and K. Shirasu (2015). "Plant cells under siege: plant immune system versus pathogen effectors." Curr Opin Plant Biol 28: 1-8.
  161. Dodds, P. N. and J. P. Rathjen (2010). "Plant immunity: towards an integrated view of plant- pathogen interactions." Nat Rev Genet 11(8): 539-548.
  162. Toruno, T. Y., I. Stergiopoulos and G. Coaker (2016). "Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners." Annu Rev Phytopathol 54: 419-441.
  163. Zipfel, C. (2014). "Plant pattern-recognition receptors." Trends Immunol 35(7): 345-351.
  164. Macho, A. P. and C. Zipfel (2014). "Plant PRRs and the activation of innate immune signaling." Mol Cell 54(2): 263-272.
  165. Svensson, B., I. Svendsen, P. Hojrup, P. Roepstorff, S. Ludvigsen and F. M. Poulsen (1992). "Primary structure of barwin: a barley seed protein closely related to the C-terminal domain of proteins encoded by wound-induced plant genes." Biochemistry 31(37): 8767-8770.
  166. Bohmer, M., T. Colby, C. Bohmer, A. Brautigam, J. Schmidt and M. Bolker (2007). "Proteomic analysis of dimorphic transition in the phytopathogenic fungus Ustilago maydis." Proteomics 7(5): 675-685.
  167. Jelenska, J., J. A. van Hal and J. T. Greenberg (2010). "Pseudomonas syringae hijacks plant stress chaperone machinery for virulence." Proc Natl Acad Sci U S A 107(29): 13177-13182.
  168. Prakash, P., B. Aruna, A. A. Sardesai and S. E. Hasnain (2005). "Purified recombinant hypothetical protein coded by open reading frame Rv1885c of Mycobacterium tuberculosis exhibits a monofunctional AroQ class of periplasmic chorismate mutase activity." J Biol Chem 280(20): 19641-19648.
  169. Kushnirov, V. V. (2000). "Rapid and reliable protein extraction from yeast." Yeast 16(9): 857-860.
  170. Blume, B., T. Nurnberger, N. Nass and D. Scheel (2000). "Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley." Plant Cell 12(8): 1425-1440.
  171. Helmstaedt, K., G. Heinrich, W. N. Lipscomb and G. H. Braus (2002). "Refined molecular hinge between allosteric and catalytic domain determines allosteric regulation and stability of fungal chorismate mutase." Proc. Natl. Acad. Sci. U.S.A. 99(10): 6631-6636.
  172. Brown, J. F. and I. W. Dawes (1990). "Regulation of chorismate mutase in Saccharomyces cerevisiae." Mol Gen Genet 220(2): 283-288.
  173. Couto, D. and C. Zipfel (2016). "Regulation of pattern recognition receptor signalling in plants." Nat Rev Immunol 16(9): 537-552.
  174. Gaffney, T., L. Friedrich, B. Vernooij, D. Negrotto, G. Nye, S. Uknes, et al. (1993). "Requirement of Salicylic-Acid for the Induction of Systemic Acquired-Resistance." Science 261(5122): 754-756.
  175. Ogino, H., T. Uchiho, J. Yokoo, R. Kobayashi, R. Ichise and H. Ishikawa (2001). "Role of intermolecular disulfide bonds of the organic solvent-stable PST-01 protease in its organic solvent stability." Appl Environ Microb 67(2): 942-947.
  176. Meinhardt, S. W., W. J. Cheng, C. Y. Kwon, C. M. Donohue and J. B. Rasmussen (2002). "Role of the arginyl-glycyl-aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis." Plant Physiol 130(3): 1545-1551.
  177. Gilroy, S., M. Bialasek, N. Suzuki, M. Gorecka, A. R. Devireddy, S. Karpinski, et al. (2016). "ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants." Plant Physiol 171(3): 1606-1615.
  178. Yamamoto, S., M. Katagiri, H. Maeno and O. Hayaishi (1965). "Salicylate Hydroxylase a Monooxygenase Requiring Flavin Adenine Dinucleotide .I. Purification General Properties." J Biol Chem 240(8): 3408-&.
  179. Vlot, A. C., D. A. Dempsey and D. F. Klessig (2009). "Salicylic Acid, a Multifaceted Hormone to Combat Disease." Annu Rev Phytopathol 47: 177-206.
  180. Dempsey, D. A., A. C. Vlot, M. C. Wildermuth and D. F. Klessig (2011). "Salicylic Acid biosynthesis and metabolism." Arabidopsis Book 9: e0156.
  181. Guyon, K., C. Balague, D. Roby and S. Raffaele (2014). "Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum." Bmc Genomics 15.
  182. Rowell, J. B. (1955). "Segregation of Sex Factors in a Diploid Line of Ustilago zeae Induced by Alpha Radiation." Science 121(3139): 304-306.
  183. Lobstein, J., C. A. Emrich, C. Jeans, M. Faulkner, P. Riggs and M. Berkmen (2012). "SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm." Microb Cell Fact 11.
  184. Nyarko, A., K. K. Singarapu, M. Figueroa, V. A. Manning, I. Pandelova, T. J. Wolpert, et al. (2014). "Solution NMR Structures of Pyrenophora tritici-repentis ToxB and Its Inactive Homolog Reveal Potential Determinants of Toxin Activity." J Biol Chem 289(37): 25946- 25956.
  185. Zhang, Z. M., X. Zhang, Z. R. Zhou, H. Y. Hu, M. L. Liu, B. Zhou, et al. (2013). "Solution structure of the Magnaporthe oryzae avirulence protein AvrPiz-t." J Biomol Nmr 55(2): 219-223.
  186. Kohler, A. C., L. H. Chen, N. Hurlburt, A. Salvucci, B. Schwessinger, A. J. Fisher, et al. (2016). "Structural Analysis of an Avr4 Effector Ortholog Offers Insight into Chitin Binding and Recognition by the Cf-4 Receptor." Plant Cell 28(8): 1945-1965.
  187. Vanholme, B., P. Kast, A. Haegeman, J. Jacob, W. Grunewald and G. Gheysen (2009). "Structural and functional investigation of a secreted chorismate mutase from the plant- parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins." Mol Plant Pathol 10(2): 189-200.
  188. Williams, S. J., K. H. Sohn, L. Wan, M. Bernoux, P. F. Sarris, C. Segonzac, et al. (2014). "Structural basis for assembly and function of a heterodimeric plant immune receptor." Science 344(6181): 299-303.
  189. Bertini, L., C. Caporale, M. Testa, S. Proietti and C. Caruso (2009). "Structural basis of the antifungal activity of wheat PR4 proteins." Febs Letters 583(17): 2865-2871.
  190. Westfall, C. S., A. Xu and J. M. Jez (2014). "Structural evolution of differential amino acid effector regulation in plant chorismate mutases." J Biol Chem 289(41): 28619-28628.
  191. El Kasmi, F. and M. T. Nishimura (2016). "Structural insights into plant NLR immune receptor function." Proc. Natl. Acad. Sci. U.S.A.
  192. Sasso, S., M. Okvist, K. Roderer, M. Gamper, G. Codoni, U. Krengel, et al. (2009). "Structure and function of a complex between chorismate mutase and DAHP synthase: efficiency boost for the junior partner." Embo J 28(14): 2128-2142.
  193. Illergard, K., D. H. Ardell and A. Elofison (2009). "Structure is three to ten times more conserved than sequence-A study of structural response in protein cores." Proteins 77(3): 499-508.
  194. Ve, T., S. J. Williams, A. M. Catanzariti, M. Rafiqi, M. Rahman, J. G. Ellis, et al. (2013). "Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant- cell entry and effector-triggered immunity." Proc. Natl. Acad. Sci. U.S.A. 110(43): 17594- 17599.
  195. Webby, C. J., W. T. Jiao, R. D. Hutton, N. J. Blackmore, H. M. Baker, E. N. Baker, et al. (2010). "Synergistic Allostery, a Sophisticated Regulatory Network for the Control of Aromatic Amino Acid Biosynthesis in Mycobacterium tuberculosis." J Biol Chem 285(40): 30567- 30576.
  196. Qamra, R., P. Prakash, B. Aruna, S. E. Hasnain and S. C. Mande (2006). "The 2.15 A crystal structure of Mycobacterium tuberculosis chorismate mutase reveals an unexpected gene duplication and suggests a role in host-pathogen interactions." Biochemistry 45(23): 6997- 7005.
  197. Trueheart, J. and I. Herskowitz (1992). "The a Locus Governs Cytoduction in Ustilago-Maydis." Journal of Bacteriology 174(23): 7831-7833.
  198. Bolker, M., M. Urban and R. Kahmann (1992). "The a mating type locus of U. maydis specifies cell signaling components." Cell 68(3): 441-450.
  199. Wiker, H. G. and M. Harboe (1992). "The Antigen-85 Complex -a Major Secretion Product of Mycobacterium-Tuberculosis." Microbiol Rev 56(4): 648-661.
  200. Daudi, A., Z. Cheng, J. A. O'Brien, N. Mammarella, S. Khan, F. M. Ausubel, et al. (2012). "The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern- triggered immunity." Plant Cell 24(1): 275-287.
  201. Soyer, J. L., A. Hamiot, B. Ollivier, M. H. Balesdent, T. Rouxel and I. Fudal (2015). "The APSES transcription factor LmStuA is required for sporulation, pathogenic development and effector gene expression in Leptosphaeria maculans." Molecular Plant Pathology 16(9): 1000-1005.
  202. Manning, V. A., S. M. Hamilton, P. A. Karplus and L. M. Ciuffetti (2008). "The Arg-Gly-Asp- containing, solvent-exposed loop of Ptr ToxA is required for internalization." Mol Plant Microbe Interact 21(3): 315-325.
  203. Catanzariti, A. M., P. N. Dodds, T. Ve, B. Kobe, J. G. Ellis and B. J. Staskawicz (2010). "The AvrM Effector from Flax Rust Has a Structured C-Terminal Domain and Interacts Directly with the M Resistance Protein." Mol Plant Microbe In 23(1): 49-57.
  204. Schulz, B., F. Banuett, M. Dahl, R. Schlesinger, W. Schafer, T. Martin, et al. (1990). "The B- Alleles of U-Maydis, Whose Combinations Program Pathogenic Development, Code for Polypeptides Containing a Homeodomain-Related Motif." Cell 60(2): 295-306.
  205. Sanchez-Vallet, A., J. R. Mesters and B. P. H. J. Thomma (2015). "The battle for chitin recognition in plant-microbe interactions." Fems Microbiol Rev 39(2): 171-183.
  206. Jashni, M. K., R. Mehrabi, J. Collemare, C. H. Mesarich and P. J. de Wit (2015). "The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant- pathogen interactions." Front Plant Sci 6: 584.
  207. Kronstad, J. W. and S. A. Leong (1990). "The B-Mating-Type Locus of Ustilago-Maydis Contains Variable and Constant Regions." Gene Dev 4(8): 1384-1395.
  208. Yamaguchi, Y., G. Pearce and C. A. Ryan (2006). "The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells." Proc. Natl. Acad. Sci. U.S.A. 103(26): 10104-10109.
  209. van Esse, H. P., M. D. Bolton, I. Stergiopoulos, P. J. G. M. de Wit and B. P. H. J. Thomma (2007). "The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor." Mol Plant Microbe In 20(9): 1092-1101.
  210. van Esse, H. P., J. W. van't Klooster, M. D. Bolton, K. A. Yadeta, P. van Baarlen, S. Boeren, et al. (2008). "The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense." Plant Cell 20(7): 1948-1963.
  211. Scherer, M., K. Heimel, V. Starke and J. Kamper (2006). "The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis." Plant Cell 18(9): 2388-2401.
  212. Xue, Y. F., W. N. Lipscomb, R. Graf, G. Schnappauf and G. Braus (1994). "The Crystal- Structure of Allosteric Chorismate Mutase at 2.2-Angstrom Resolution." Proc. Natl. Acad. Sci. U.S.A. 91(23): 10814-10818.
  213. Goers, S. K. and R. A. Jensen (1984). "The differential allosteric regulation of two chorismate- mutase isoenzymes of Nicotiana silvestris." Planta 162(2): 117-124.
  214. Calhoun, D. H., C. A. Bonner, W. Gu, G. Xie and R. A. Jensen (2001). "The emerging periplasm- localized subclass of AroQ chorismate mutases, exemplified by those from Salmonella typhimurium and Pseudomonas aeruginosa." Genome Biol 2(8): RESEARCH0030.
  215. Puhalla, J. E. (1969). "The formation of diploids of Ustilago maydis on agar medium." Phytopathology 59(11): 1771-1772.
  216. Ciacci, C., I. Russo, C. Bucci, P. Iovino, L. Pellegrini, I. Giangrieco, et al. (2014). "The kiwi fruit peptide kissper displays anti-inflammatory and anti-oxidant effects in in-vitro and ex- vivo human intestinal models." Clin Exp Immunol 175(3): 476-484.
  217. Dai, L. M., D. Wang, X. Q. Xie, C. H. Zhang, X. P. Wang, Y. Xu, et al. (2016). "The Novel Gene VpPR4-1 from Vitis pseudoreticulata Increases Powdery Mildew Resistance in Transgenic Vitis vinifera L." Frontiers in Plant Science 7.
  218. Hartmann, H. A., R. Kahmann and M. Bolker (1996). "The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis." Embo J 15(7): 1632-1641.
  219. Jones, J. D. and J. L. Dangl (2006). "The plant immune system." Nature 444(7117): 323-329.
  220. Papaleo, E., G. Saladino, M. Lambrughi, K. Lindorff-Larsen, F. L. Gervasio and R. Nussinov (2016). "The Role of Protein Loops and Linkers in Conformational Dynamics and Allostery." Chem Rev 116(11): 6391-6423.
  221. Mukamolova, G. V., O. A. Turapov, K. Kazarian, M. Telkov, A. S. Kaprelyants, D. B. Kell, et al. (2002a). "The rpf gene of Micrococcus luteus encodes an essential secreted growth factor." Mol Microbiol 46(3): 611-621.
  222. Yu, X. L., J. L. Tang, Q. Q. Wang, W. W. Ye, K. Tao, S. Y. Duan, et al. (2012). "The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death." New Phytol 196(1): 247-260.
  223. Maeda, H. and N. Dudareva (2012). "The Shikimate Pathway and Aromatic Amino Acid Biosynthesis in Plants." Annual Review of Plant Biology 63(1): 73-105.
  224. Dean, R., J. A. Van Kan, Z. A. Pretorius, K. E. Hammond-Kosack, A. Di Pietro, P. D. Spanu, et al. (2012). "The Top 10 fungal pathogens in molecular plant pathology." Mol Plant Pathol 13(4): 414-430.
  225. Dong, S. M., S. Raffaele and S. Kamoun (2015). "The two-speed genomes of filamentous pathogens: waltz with plants." Curr Opin Genet Dev 35: 57-65.
  226. Gongora-Castillo, E., E. Ibarra-Laclette, D. L. Trejo-Saavedra and R. F. Rivera-Bustamante (2012). "Transcriptome analysis of symptomatic and recovered leaves of geminivirus- infected pepper (Capsicum annuum)." Virol J 9.
  227. Grandaubert, J., R. G. T. Lowe, J. L. Soyer, C. L. Schoch, A. P. V. de Wouw, I. Fudal, et al. (2014). "Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens." Bmc Genomics 15.
  228. Zhang, M. X., Q. Li, T. L. Liu, L. Liu, D. Y. Shen, Y. Zhu, et al. (2015). "Two Cytoplasmic Effectors of Phytophthora sojae Regulate Plant Cell Death via Interactions with Plant Catalases." Plant Physiol 167(1): 164-175.
  229. Liu, T. L., W. W. Ye, Y. Y. Ru, X. Y. Yang, B. A. Gu, K. Tao, et al. (2011). "Two Host Cytoplasmic Effectors Are Required for Pathogenesis of Phytophthora sojae by Suppression of Host Defenses." Plant Physiol 155(1): 490-501.
  230. Doehlemann, G., S. Reissmann, D. Assmann, M. Fleckenstein and R. Kahmann (2011). "Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation." Mol Microbiol 81(3): 751-766.
  231. Schnappauf, G., S. Krappmann and G. H. Braus (1998). "Tyrosine and tryptophan act through the same binding site at the dimer interface of yeast chorismate mutase." J Biol Chem 273(27): 17012-17017.
  232. Liu, T. L., T. Q. Song, X. Zhang, H. B. Yuan, L. M. Su, W. L. Li, et al. (2014). "Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis." Nat Commun 5.
  233. Martin, F., A. Kohler, C. Murat, C. Veneault-Fourrey and D. S. Hibbett (2016). "Unearthing the roots of ectomycorrhizal symbioses." Nat Rev Microbiol 14(12): 760-773.
  234. Brefort, T., G. Doehlemann, A. Mendoza-Mendoza, S. Reissmann, A. Djamei and R. Kahmann (2009). "Ustilago maydis as a Pathogen." Annu Rev Phytopathol 47: 423-445.
  235. Holliday, R. (1974). Ustilago maydis. Bacteria, Bacteriophages, and Fungi. R. C. King. Boston, MA, Springer US. 1: 575-595.
  236. Lanver, D., M. Tollot, G. Schweizer, L. Lo Presti, S. Reissmann, L. S. Ma, et al. (2017). "Ustilago maydis effectors and their impact on virulence." Nat Rev Microbiol 15(7): 409- 421.
  237. Snetselaar, K. M., M. Bolker and R. Kahmann (1996). "Ustilago maydis mating hyphae orient their growth toward pheromone sources." Fungal Genetics and Biology 20(4): 299-312.
  238. Kahmann, R., G. Steinberg, C. Basse, M. Feldbrügge and J. Kämper (2000). Ustilago maydis, the Causative Agent of Corn Smut Disease. Fungal Pathology. J. W. Kronstad. Dordrecht, Springer Netherlands: 347-371.
  239. Santhanam, P. and B. P. H. J. Thomma (2013). "Verticillium dahliae Sge1 Differentially Regulates Expression of Candidate Effector Genes." Mol Plant Microbe In 26(2): 249-256.
  240. Raab-Traub, N. and D. P. Dittmer (2017). "Viral effects on the content and function of extracellular vesicles." Nat Rev Microbiol 15(9): 559-572.
  241. Forrellad, M. A., L. I. Klepp, A. Gioffre, J. S. Y. Garcia, H. R. Morbidoni, M. D. Santangelo, et al. (2013). "Virulence factors of the Mycobacterium tuberculosis complex." Virulence 4(1): 3-66.
  242. Caporale, C., I. Di Berardino, L. Leonardi, L. Bertini, A. Cascone, V. Buonocore, et al. (2004). "Wheat pathogenesis-related proteins of class 4 have ribonuclease activity." Febs Letters 575(1-3): 71-76.
  243. Schmidheini, T., H. U. Mosch, J. N. Evans and G. Braus (1990). "Yeast allosteric chorismate mutase is locked in the activated state by a single amino acid substitution." Biochemistry 29(15): 3660-3668.

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